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Influence of an extreme climatic event on bilateral asymmetry and occurrence of eye flukes in perch (Perca fluviatilis) and roach (Rutilus rutilus) from a lake in southeast England

Published online by Cambridge University Press:  28 June 2019

N.J. Morley*
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham TW20 0EX, UK
J.W. Lewis
Affiliation:
School of Biological Sciences, Royal Holloway, University of London, Egham TW20 0EX, UK
*
Author for correspondence: Neil J. Morley, E-mail: n.morley@rhul.ac.uk

Abstract

Eye flukes are common infections of freshwater fish and their occurrence as metacercarial stages may occur non-randomly resulting in an asymmetrical distribution within the host eyes. However, from previous studies the presentation of bias by these trematodes lacks consistency suggesting that congenital asymmetrical effects are unlikely to be the cause and exogenous factors, such as environmental stress, may be more influential. The present study, undertaken over a 4-year period, investigates the impact of an extreme heatwave and drought on the annual bilateral asymmetry and occurrence of two eye fluke species (Diplostomum sp. in the lens and Tylodelphys sp. in the vitreous humour) from perch (Perca fluviatilis) and roach (Rutilus rutilus). The onset of the extreme climatic event resulted in a significant negative effect on the occurrence of the eye flukes. Bilateral asymmetry, which was present within both trematode species and hosts, appeared to be highly variable between eye fluke and fish species and also year of study. However, during the pre-drought period both host species demonstrated significant asymmetry for Tylodelphys sp. but not for Diplostomum sp. while during the drought this bias was reversed. The potential role of fluctuating asymmetry of fish hosts in structuring the bilateral asymmetry of eye flukes is discussed.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

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References

Allenbach, DM (2011) Fluctuating asymmetry and exogenous stress in fishes: a review. Reviews of Fish Biology and Fisheries 21, 355376.Google Scholar
Blair, D (1977) A key to cercariae of British strigeoids (Digenea) for which the life-cycles are known, and notes on the characters used. Journal of Helminthology 51, 155166.Google Scholar
Bouillon, DR and Curtis, MA (1987) Diplostomiasis (Trematoda: Strigeidae) in arctic charr (Salvelinus alpinus) from Charr lake, northern Labrador. Journal of Wildlife Diseases 23, 502505.Google Scholar
Burrough, RJ (1978) The population biology of two species of eyefluke, Diplostomum spathaceum and Tylodelphys clavata, in roach and rudd. Journal of Fish Biology 13, 1932.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.Google Scholar
Chappell, LH (1969) The parasites of the three-spined stickleback Gasterosteus aculeatus L. from a Yorkshire pond: 1. Seasonal variation of parasite fauna. Journal of Fish Biology 1, 137152.Google Scholar
Chappell, LH (1995) The biology of diplostomatid eyeflukes of fishes. Journal of Helminthology 69, 97101.Google Scholar
Ching, HL (1985) Occurrence of the eye fluke, Diplostomum (Diplostomum) baeri bucculentum Dubois et Rausch 1948, in salmonid fishes of northern British Columbia. Canadian Journal of Zoology 63, 396399.Google Scholar
Estes, ECJ, Katholi, CR and Angus, RA (2006) Elevated fluctuating asymmetry in eastern mosquitofish (Gambusia holbrooki) from a river receiving paper mill effluent. Environmental Toxicology & Chemistry 25, 10261033.Google Scholar
Graczyk, T (1991) Cases of bilateral asymmetry of Diplostomum pseudosapthaceum Niewiadomska, 1984 metacercariae infections (Trematoda: Diplostomatidae) in the eye lens of fish. Acta Parasitologica Polonica 36, 131134.Google Scholar
Haas, W, Wulff, C, Grabe, K, Meyer, V and Haeberlein, S (2007) Navigation within host tissues: cues for orientation of Diplostomum spathaceum (Trematoda) in fish towards vein, head and eye. Parasitology 134, 10131023.Google Scholar
Höglund, J (1991) Untrastructural observations and radiometric assay on cercarial penetration and migration of the digenean Diplostomum spathaceum in the rainbow trout Oncorhynchus mykiss. Parasitology Research 77, 283289.Google Scholar
Hulme, M (1997) The climate in the UK from November 1994 to October 1995. Weather 52, 242257.Google Scholar
Johnson, KA (1971) The migration of Cotylurus erraticus cercariae (Trematoda: Strigeidae) in rainbow trout (Salmo gairdneri) and their effects on the host. Journal of Parasitology 57, 244251.Google Scholar
Johnson, PTJ, Koprivnikar, J, Orlofske, SA, Melbourne, BA and Lafonte, BE (2014) Making the right choice: testing the drivers of asymmetric infections within hosts and their consequences for pathology. Oikos 123, 875885.Google Scholar
Karvonen, A (2012) Diplostomum spathaceum and related species. pp. 260269 in Woo, PTK and Buchmann, K (Eds) Fish parasites: Pathobiology and protection. Wallingford, CABI.Google Scholar
Karvonen, A and Seppälä, O (2008) Eye fluke infection and lens size reduction in fish: a quantitative analysis. Diseases of Aquatic Organisms 80, 2126.Google Scholar
Machado, PM, Takemoto, RM and Pavenelli, GC (2005) Diplostomum (Austrodiplostomum) compactum (Lutz, 1928) (Platyhelminthes, Digenea) metacercariae in fish from the floodplain of the Upper Paraná, Brazil. Parasitology Research 97, 436444.Google Scholar
Marsh, T, Cole, G and Wilby, R (2007) Major droughts in England and Wales, 1800–2006. Weather 62, 8793.Google Scholar
Morley, NJ and Lewis, JW (2014) Extreme climatic events and host-pathogen interactions: the impact of the 1976 drought in the UK. Ecological Complexity 17, 119.Google Scholar
Morley, NJ and Lewis, JW (2019) Influence of Ligula intestinalis plerocercoids (Cestoda: Diphyllobothriidae) on the occurrence of eyeflukes in roach (Rutilus rutilus) from a lake in south-east England. Journal of Helminthology 93, 6670.Google Scholar
Muzzall, PM and Peebles, CR (1987) Parasites of the emerald shiner, Notropis atherinoides, from two localities in the St. Marys River, Michigan with emphasis on larval trematodes. Proceedings of the Helminthological Society of Washington 54, 105110.Google Scholar
Muzzall, PM and Peebles, CR (1988) Helminths of rainbow smelt, Osmerus mordax, from five localities in Lake Huron and Lake Michigan, with emphasis on Diplostomum spathaceum. Proceedings of the Helminthological Society of Washington 55, 281285.Google Scholar
National Rivers Authority (1995) The drought of 1995. National Rivers Authority, Bristol.Google Scholar
Pennycuick, L (1971) Seasonal variations in the parasite infections in a population of three-spined sticklebacks, Gasterosteus aculeatus L. Parasitology 63, 373388.Google Scholar
Rau, ME, Gordon, DM and Curtis, MA (1979) Bilateral asymmetry of Diplostomum infections in the eyes of lake whitefish Coregonus chipeaformis (Mitchell) and a computer simulation of the observed metacercarial distribution. Journal of Fish Diseases 2, 291297.Google Scholar
Reiczigel, J and Rozsa, L (2005) Quantitative parasitology 3.0. Budapest. Distributed by the authors.Google Scholar
Rintamäki-Kinnunen, P, Karvonen, A, Anttila, P and Valtonen, ET (2004) Diplostomum spathaceum metacercarial infection and colour change in salmonid fish. Parasitology Research 93, 5155.Google Scholar
Shaw, JC, Aguirre-Macedo, L and Lafferty, KD (2005) An efficient strategy to estimate intensity and prevalence: sampling metacercariae in fishes. Journal of Parasitology 91, 515521.Google Scholar
Shigin, AA (1964) The life span of Diplostomum spathaceum in the intermediate host. Trudy Gel'mintologicheskoi Laboratorii Akademiya Nauk SSSR 14, 262272 (in Russian).Google Scholar
Thompson, RD (1996) The weather at Reading during 1995. Reading Naturalist 48, 4550.Google Scholar
Vidal-Martinez, VM, Pech, D, Sures, B, Purucker, ST and Poulin, R (2010) Can parasites really reveal environmental impact? Trends in Parasitology 26, 4451.Google Scholar
Wayland, MT and Chubb, JC (2016) A new R package and web application for detecting bilateral asymmetry in parasitic infections. Folia Parasitologica 63, 039.Google Scholar
Whyte, SK, Secombes, CJ and Chappell, LH (1991) Studies on the infectivity of Diplostomum spathaceum in rainbow trout (Oncorhynchus mykiss). Journal of Helminthology 65, 169178.Google Scholar
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